Intergenerational transmission of sociality: the role of parents in shaping social behavior in monogamous and non-monogamous species

Abstract

Social bonds are necessary for many mammals to survive and reproduce successfully. These bonds (i.e. pair-bonds, friendships, filial bonds) are characterized by different periods of development, longevity and strength. Socially monogamous species display certain behaviors not seen in many other mammals, such as adult pairbonding and male parenting. In our studies of prairie voles (Microtus ochrogaster) and titi monkeys (Callicebus cupreus), we have examined the neurohormonal basis of these bonds. Here, we discuss the evidence from voles that aspects of adolescent and adult social behavior are shaped by early experience, including changes to sensory systems and connections, neuropeptide systems such as oxytocin and vasopressin, and alterations in stress responses. We will compare this with what is known about these processes during development and adulthood in other mammalian species, both monogamous and non-monogamous, and how our current knowledge in voles can be used to understand the development of and variation in social bonds. Humans are endlessly fascinated by the variety of social relationships and family types displayed by animal species, including our own. Social relationships can be characterized by directionality (either uni-or bi-directional), longevity, developmental epoch (infant, juvenile or adult) and strength. Research on the neurobiology of social bonds in animals has focused primarily on 'socially monogamous' species, because of their long-term, strong adult affiliative bonds. In this Review, we attempt to understand how the ability and propensity to form these bonds (or lack thereof), as well as the display of social behaviors more generally, are transmitted both genomically and non-genomically via variation in parenting in monogamous and non-monogamous species.

Multimodal pair‐bond maintenance: A review of signaling across modalities in pair‐bonded nonhuman primates

“…We note instances where signal use differs by sex within a species, which may suggest which sex is primarily responsible for maintaining and/or advertising the pair‐bond, or alternatively which modalities are preferentially exhibited by which sex (an area in need of further research). Ultimately, multiple modalities may be used to reinforce a single piece of communication—“we are pair‐bonded and this is our territory.” While neuroendocrine signals also play a prominent role in pair‐bonding (and biparental care), this signaling system lies outside the scope of this paper and has been extensively reviewed within the existing literature (for recent reviews see: French et al, 2018; Lieberwirth & Wang, 2016; Perkeybile & Bales, 2017; Storey & Ziegler, 2016; Ziegler & Crockford, 2017).…”

“…Ultimately, multiple modalities may be used to reinforce a single piece of communication-"we are pair-bonded and this is our territory." While neuroendocrine signals also play a prominent role in pair-bonding (and biparental care), this signaling system lies outside the scope of this paper and has been extensively reviewed within the existing literature (for recent reviews see: French et al, 2018;Lieberwirth & Wang, 2016;Perkeybile & Bales, 2017;Storey & Ziegler, 2016;Ziegler & Crockford, 2017).…”

Paternal Care in Biparental Rodents: Intra- and Inter-individual Variation

“…1). Numerous correlational and experimental studies in the prairie vole, meadow vole, mandarin vole, and California mouse (reviewed by Frazier et al 2006;Bales and Saltzman 2016;Perkeybile and Bales 2017) have implicated AVP, especially vasopressinergic projections from the MeA and BNST to the LS and LHN, in regulating paternal care. The experiments reviewed above further indicate that AVP signaling is altered by several experiential factors that simultaneously influence paternal behavior.…”

Parenting in animals

“…More recently, the effects of parenting have also been studied in a socially monogamous, biparental species, the prairie vole ( Microtus ochrogaster ) [44]. Vole parents were classified into high, medium, and low contact pairs [45].…”